Memory enhancement of fresh ginseng on deficits induced by chronic restraint stress in mice

References

• Van den Hove DL, Blanco CE, Aendekerk B, Desbonnet L, Bruschettini M, Steinbusch HP, et al. Prenatal restraint stress and long-term affective consequences. Dev Neurosci 2005;27(5):313–20.
   PubMed Web of Science ®Google Scholar
• Budni J, Zomkowski AD, Engel D, Santos DB, Dos Santos AA, Moretti M, et al. Folic acid prevents depressive-like behavior and hippocampal antioxidant imbalance induced by restraint stress in mice. Exp Neurol 2013;240:112–21. doi:10.1016/j.expneurol.2012.10.024
   PubMed Web of Science ®Google Scholar
• Camila OA, Gislaine ZR, Helena MA, Karine FR, Amanda VS, Francielle M, et al. Synergist effects of n-acetylcysteine and deferoxamine treatment on behavioral and oxidative parameters induced by chronic mild stress in rats. Neurochem Int 2012;61:1072–80. doi:10.1016/j.neuint.2012.07.024.
   PubMed Web of Science ®Google Scholar
• Tian X, Sun L, Gou L, Ling X, Feng Y, Wang L, et al. Protective effect of L-theanine on chronic restraint stress-induced cognitive impairments in mice. Brain Res 2013;1503:24–32. doi:10.1016/j.brainres.2013.01.048
   PubMed Web of Science ®Google Scholar
• Forstmann BU, Wagenmakers EJ, Eichele T, Brown S, Serences JT. Reciprocal relations between cognitive neuroscience and cognitive models: opposites attract? Trends Cogn Sci 2011;15(6):272–9. doi:10.1016/j.tics.2011.04.002
   PubMed Web of Science ®Google Scholar
• Gagné RM. Learning outcomes and their effects: useful categories of human performance. Am Psychol 1984;39(4):377–385.
   Web of Science ®Google Scholar
• Huang RR, Hu W, Yin YY, Wang YC, Li WP, Li WZ. Chronic restraint stress promotes learning and memory impairment due to enhanced neuronal endoplasmic reticulum stress in the frontal cortex and hippocampus in male mice. Int J Mol Med 2015;35(2):553–9. doi:10.3892/ijmm.2014.2026
   PubMed Web of Science ®Google Scholar
• Huang P, Li C, Fu T, Zhao D, Yi Z, Lu Q, et al. Flupirtine attenuates chronic restraint stress-induced cognitive deficits and hippocampal apoptosis in male mice. Behav Brain Res 2015;288:1–10. doi:10.1016/j.bbr.2015.04.004
   PubMed Web of Science ®Google Scholar
• Wang KZ, Xu P, Lu C, Dong LM, Zhang BY, Liu XM, et al. Effects of ginsenoside Rg1 on learning and memory in a reward-directed instrumental conditioning task in chronic restraint stressed rats. Phytother Res 2017;31(1):81–9. doi:10.1002/ptr.5733
   PubMed Web of Science ®Google Scholar
• Langley B, Ratan RR. Oxidative stress-induced death in the nervous system: cell cycle dependent or independent?. J Neurosci Res 2004;77(5):621–9.
   PubMed Web of Science ®Google Scholar
• Kumar RS, Narayanan SN, Nayak S. Ascorbic acid protects against restraint stress-induced memory deficits in wistar rats. Clinics (Sao Paulo) 2009;64(12):1211–7. doi:10.1590/S1807-59322009001200012
   PubMed Web of Science ®Google Scholar
• Zhao HF, Li Q, Li Y. Long-term ginsenoside administration prevents memory loss in aged female C57BL/6J mice by modulating the redox status and up-regulating the plasticity-related proteins in hippocampus. Neuroscience 2011;183:189–202. doi:10.1016/j.neuroscience.2011.03.048
   PubMed Web of Science ®Google Scholar
• Madrigal JL, Olivenza R, Moro MA, Lizasoain I, Lorenzo P, Rodrigo J, et al. Glutathione depletion, lipid peroxidation and mitochondrial dysfunction are induced by chronic stress in rat brain. Neuropsychopharmacology 2001;24(4):420–9.
   PubMed Web of Science ®Google Scholar
• Kuang H, Sun M, Lv J, Li J, Wu C, Chen N, et al. Hippocampal apoptosis involved in learning deficits in the offspring exposed to maternal high sucrose diets. J Nutr Biochem 2014;25:985–90. doi:10.1016/j.jnutbio.2014.04.012
   PubMed Web of Science ®Google Scholar
• Lucassen PJ, Heine VM, Muller MB, van der Beek EM, Wiegant VM, De Kloet ER, et al. Stress, depression and hippocampal apoptosis. CNS Neurol Disord Drug Targets 2006;5(5):531–46.
   PubMedGoogle Scholar
• Zhang Y, Liu W, Zhou Y, Ma C, Li S, Cong B. Endoplasmic reticulum stress is involved in restraint stress-induced hippocampal apoptosis and cognitive impairments in rats. Physiol Behav 2014;131:41–8. doi:10.1016/j.physbeh.2014.04.014
   PubMed Web of Science ®Google Scholar
• Lucca G, Comim CM, Valvassori SS, Réus GZ, Vuolo F, Petronilho F, et al. Effects of chronic mild stress on the oxidative parameters in the rat brain. Neurochem Int 2009;54(5–6):358–62. doi:10.1016/j.neuint.2009.01.001
   PubMed Web of Science ®Google Scholar
• Gupta V, Lahiri SS, Sultana S, Tulsawani RK, Kumar R. Anti-oxidative effect of Rhodiola imbricata root extract in rats during cold, hypoxia and restraint (C-H-R) exposure and post-stress recovery. Food Chem Toxicol 2010;48(4):1019–25. doi:10.1016/j.fct.2010.01.012
   PubMed Web of Science ®Google Scholar
• Dang HX, Sun LH, Liu XM, Peng B, Wang Q, Willaim J, et al. Preventive action of Kai Xin San aqueous extract on depressive-like symptoms and cognition deficit induced by chronic mild stress. Exp Biol Med (Maywood) 2009;234(7):785–93. doi:10.3181/0812-RM-354
   PubMed Web of Science ®Google Scholar
• Nama Y, Wieb MB, Shina EJ, Nguyena TL, Nahc SY, Kod SK, et al. Ginsenoside Re protects methamphetamine-induced mitochondrial burdens and proapoptosis via genetic inhibition of protein kinase C δ in human neuroblastoma dopaminergic SH-SY5Y cell lines. J Appl Toxicol 2015;35:927–44. doi:10.1002/jat.3093
   PubMed Web of Science ®Google Scholar
• Liu JF, Yan XD, Qi LS, Li L, Hu GY, Li P, et al. Ginsenoside Rd attenuates Aβ25–35-induced oxidative stress and apoptosis in primary cultured hippocampal neurons. Chem Biol Interact 2015;239:12–8. doi:10.1016/j.cbi.2015.06.030
   PubMed Web of Science ®Google Scholar
• López MV, Cuadrado MP, Ruiz-Poveda OM, Del Fresno AM, Accame ME. Neuroprotective effect of individual ginsenosides on astrocytes primary culture. Biochim Biophys Acta 2007;1770(9):1308–16.
   PubMed Web of Science ®Google Scholar
• Wang J, Sun C, Zheng Y, Pan H, Zhou Y, Fan Y. The effective mechanism of the polysaccharides from Panax ginseng on chronic fatigue syndrome. Arch Pharm Res 2014;37(4):530–8. doi:10.1007/s12272-013-0235-y
   PubMed Web of Science ®Google Scholar
• Jiang YM, Li ZY, Liu XM, Chang Q, Zhang J, Pan RL. Comparative study on neuroprotective effect of dry and fresh Panax ginseng against the damage in PC12 cells. Nat Prod Res Dev 2014;26:1072–6.
   Google Scholar
• Wang Y, Lu C, Song GQ, Chen YX, Wu HW, Wang Q, et al. Effects of chronic restraint stress on learning and memory in SD and wistar rats. Acta Lab Anim Sci Sin 2014;22(2):40–44.
   Google Scholar
• Nagata K, Nakashima-Kamimura N, Mikami T, Ohsawa I, Ohta S. Consumption of molecular hydrogen prevents the stress-induced impairments in hippocampus-dependent learning tasks during chronic physical restraint in mice. Neuropsychopharmacology 2009;34(2):501–8. doi:10.1038/npp.2008.95
   PubMed Web of Science ®Google Scholar
• González-Burgos E, Fernandez-Moriano C, Gómez-Serranillos MP. Potential neuroprotective activity of Ginseng in Parkinson’s disease: a review. J Neuroimmune Pharmacol 2015;10(1):14–29. doi:10.1007/s11481-014-9569-6
   PubMed Web of Science ®Google Scholar
• Sunwoo HH, Kim CT, Kim DY, Maeng JS, Cho CW, Lee SJ. Extraction of ginsenosides from fresh ginseng roots (Panax ginseng C.A. Meyer) using commercial enzymes and high hydrostatic pressure. Biotechnol Lett 2013;35(7):1017–22. doi:10.1007/s10529-013-1182-x
   PubMed Web of Science ®Google Scholar
• Ji YC, Kim YB, Park SW, Hwang SN, Min BK, Hong HJ, et al. Neuroprotective effect of ginseng total saponins in experimental traumatic brain injury. J Korean Med Sci 2005;20(2):291–6.
   PubMed Web of Science ®Google Scholar
• Hu BY, Liu XJ, Qiang R, Jiang ZL, Xu LH, Wang GH, et al. Treatment with ginseng total saponins improves the neurorestoration of rat after traumatic brain injury. J Ethnopharmacol 2014;155(2):1243–55. doi:10.1016/j.jep.2014.07.009
   PubMed Web of Science ®Google Scholar
• Lu C, Shi Z, Dong L, Lv J, Xu P, Li Y, et al. Exploring the effect of ginsenoside Rh1 in a sleep deprivation-induced mouse memory impairment model. Phytother Res 2017;31(5):763–70. doi:10.1002/ptr.5797
   PubMed Web of Science ®Google Scholar
• Bevins RA, Besheer J. Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study “recognition memory”. Nat Protoc 2006;1(3):1306–11.
   PubMed Web of Science ®Google Scholar
• Dong X, Zheng L, Lu S, Yang Y. Neuroprotective effects of pretreatment of ginsenoside Rb1 on severe cerebral ischemia-induced injuries in aged mice: involvement of anti-oxidant signaling. Geriatr Gerontol Int 2017;17(2):338–45. doi:10.1111/ggi.12699
   PubMed Web of Science ®Google Scholar
• Liu Z, Xia J, Wang CZ, Zhang JQ, Ruan CC, Sun GZ, et al. Remarkable impact of acidic ginsenosides and organic acids on ginsenoside transformation from fresh ginseng to red ginseng. J Agric Food Chem 2016;64(26):5389–99. doi:10.1021/acs.jafc.6b00963
   PubMed Web of Science ®Google Scholar
• Wang YS, Jin YP, Gao W, Xiao SY, Zhang YW, Zheng PH, et al. Complete 1H-NMR and 13C-NMR spectral assignment of five malonyl ginsenosides from the fresh flower buds of Panax ginseng. J Ginseng Res 2016;40(3):245–50. doi:10.1016/j.jgr.2015.08.003
   PubMed Web of Science ®Google Scholar
• Liu ZQ, Luo XY, Liu GZ, Chen YP, Wang ZC, Sun YX. In vitro study of the relationship between the structure of ginsenoside and its antioxidative or prooxidative activity in free radical induced hemolysis of human erythrocytes. J Agric Food Chem 2003;51(9):2555–8.
   PubMed Web of Science ®Google Scholar
• Ennaceur A, Michalikova S, Bradford A, Ahmed S. Detailed analysis of the behavior of lister and wistar rats in anxiety, object recognition and object location tasks. Behav Brain Res 2005;159(2):247–66.
   PubMed Web of Science ®Google Scholar
• Winters BD, Bussey TJ. Glutamate receptors in perirhinal cortex mediate encoding, retrieval, and consolidation of object recognition memory. J Neurosci 2005;25(17):4243–51.
   PubMed Web of Science ®Google Scholar
• Silvers JM, Harrod SB, Mactutus CF, Booze RM. Automation of the novel object recognition task for use in adolescent rats. J Neurosci Methods 2007;166(1):99–103.
   PubMed Web of Science ®Google Scholar
• Li S, Fan YX, Wang W, Tang YY. Effects of acute restraint stress on different components of memory as assessed by object-recognition and object-location tasks in mice. Behav Brain Res 2012;227(1):199–207. doi:10.1016/j.bbr.2011.10.007
   PubMed Web of Science ®Google Scholar
• Conrad CD, McLaughlin KJ, Huynh TN, El-Ashmawy M, Sparks M. Chronic stress and a cyclic regimen of estradiol administration separately facilitate spatial memory: relationship with hippocampal CA1 spine density and dendritic complexity. Behav Neurosci 2012;126(1):142–56. doi:10.1037/a0025770
   PubMed Web of Science ®Google Scholar
• Meiri N, Rosenblum K. Lateral ventricle injection of the protein synthesis inhibitor anisomycin impairs long-term memory in a spatial memory task. Brain Res 1998;789(1):48–55.
   PubMed Web of Science ®Google Scholar
• Matsumoto K, Yobimoto K, Huong NT, Abdel-Fattah M, Van Hien T, Watanabe H. Psychological stress-induced enhancement of brain lipid peroxidation via nitric oxide systems and its modulation by anxiolytic and anxiogenic drugs in mice. Brain Res 1999;839(1):74–84.
   PubMed Web of Science ®Google Scholar
• Shaheen AA, Hamdy MA, Kheir-Eldin AA, Lindström P, el-Fattah AA. Effect of pretreatment with vitamin E or diazepam on brain metabolism of stressed rats. Biochem Pharmacol 1993;46(1):194–7.
   PubMed Web of Science ®Google Scholar
• Jangra A, Sriram CS, Dwivedi S, Gurjar SS, Hussain MI, Borah P, et al. Sodium phenylbutyrate and edaravone abrogate chronic restraint stress-induced behavioral deficits: implication of oxido-nitrosative, endoplasmic reticulum stress cascade, and neuroinflammation. Cell Mol Neurobiol 2017;37(1):65–81. doi:10.1007/s10571-016-0344-5
   PubMed Web of Science ®Google Scholar
• Samarghandian S, Farkhondeh T, Samini F, Borji A. Protective effects of carvacrol against oxidative stress induced by chronic stress in rat’s brain, liver, and kidney. Biochem Res Int 2016;2016:2645237. doi:10.1155/2016/2645237
   PubMed Web of Science ®Google Scholar
• Balu M, Sangeetha P, Murali G, Panneerselvam C. Age-related oxidative protein damages in central nervous system of rats: modulatory role of grape seed extract. Int J Dev Neurosci 2005;23(6):501–7.
   PubMed Web of Science ®Google Scholar
• Bhat MS, Rao G, Murthy KD, Bhat PG. Housing in pyramid counteracts neuroendocrine and oxidative stress caused by chronic restraint in rats. Evid Based Complement Alternat Med 2007;4(1):35–42.
   PubMed Web of Science ®Google Scholar
• Fontella FU, Siqueira IR, Vasconcellos AP, Tabajara AS, Netto CA, Dalmaz C. Repeated restraint stress induces oxidative damage in rat hippocampus. Neurochem Res 2005;30(1):105–11.
   PubMed Web of Science ®Google Scholar
• Sandhir R, Julka D, Gill KD. Lipoperoxidative damage on lead exposure in rat brain and its implications on membrane bound enzymes. Pharmacol Toxicol 1994;74(2):66–71.
   PubMedGoogle Scholar